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Title: Comparative genomics reveals unique wood-decay strategies and fruiting body development in the Schizophyllaceae

Abstract

Agaricomycetes are fruiting body-forming fungi that produce some of the most efficient enzyme systems to degrade wood. Despite decades-long interest in their biology, the evolution and functional diversity of both wood-decay and fruiting body formation are incompletely known. We performed comparative genomic and transcriptomic analyses of wood-decay and fruiting body development in Auriculariopsis ampla and Schizophyllum commune (Schizophyllaceae), species with secondarily simplified morphologies, an enigmatic wood-decay strategy and weak pathogenicity to woody plants. The plant cell wall-degrading enzyme repertoires of Schizophyllaceae are transitional between those of white rot species and less efficient wood-degraders such as brown rot or mycorrhizal fungi. Rich repertoires of suberinase and tannase genes were found in both species, with tannases restricted to Agaricomycetes that preferentially colonize bark-covered wood, suggesting potential complementation of their weaker wood-decaying abilities and adaptations to wood colonization through the bark. Fruiting body transcriptomes revealed a high rate of divergence in developmental gene expression, but also several genes with conserved expression patterns, including novel transcription factors and small-secreted proteins, some of the latter which might represent fruiting body effectors. Finally, taken together, our analyses highlighted novel aspects of wood-decay and fruiting body development in an important family of mushroom-forming fungi.

Authors:
 [1];  [1];  [1];  [1]; ORCiD logo [2];  [1];  [3];  [4]; ORCiD logo [5];  [3];  [6];  [6];  [6];  [6];  [6]; ORCiD logo [6]; ORCiD logo [1]
  1. Biological Research Center, Szeged (Hungary)
  2. Eötvös Loránd Univ., Budapest (Hungary); Hungarian Academy of Sciences, Budapest (Hungary)
  3. Seqomics Ltd., Mórahalom (Hungary)
  4. Univ. Aix‐Marseille, Marseille (France); INRA, Marseille (France)
  5. Univ. Aix‐Marseille, Marseille (France); INRA, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Hungary Academy of Sciences; European Research Council (ERC); National Research, Development and Innovation office
OSTI Identifier:
1619130
Alternate Identifier(s):
OSTI ID: 1545936
Grant/Contract Number:  
AC02-05CH11231; LP2014/12; 758161; Ginop-2.3.2-15-00002; AC02‐05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 224; Journal Issue: 2; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bark degredation; fruiting body development; genome; mushroom-forming fungi

Citation Formats

Almási, Éva, Sahu, Neha, Krizsán, Krisztina, Bálint, Balázs, Kovács, Gábor M., Kiss, Brigitta, Cseklye, Judit, Drula, Elodie, Henrissat, Bernard, Nagy, István, Chovatia, Mansi, Adam, Catherine, LaButti, Kurt, Lipzen, Anna, Riley, Robert, Grigoriev, Igor V., and Nagy, László G. Comparative genomics reveals unique wood-decay strategies and fruiting body development in the Schizophyllaceae. United States: N. p., 2019. Web. doi:10.1111/nph.16032.
Almási, Éva, Sahu, Neha, Krizsán, Krisztina, Bálint, Balázs, Kovács, Gábor M., Kiss, Brigitta, Cseklye, Judit, Drula, Elodie, Henrissat, Bernard, Nagy, István, Chovatia, Mansi, Adam, Catherine, LaButti, Kurt, Lipzen, Anna, Riley, Robert, Grigoriev, Igor V., & Nagy, László G. Comparative genomics reveals unique wood-decay strategies and fruiting body development in the Schizophyllaceae. United States. https://doi.org/10.1111/nph.16032
Almási, Éva, Sahu, Neha, Krizsán, Krisztina, Bálint, Balázs, Kovács, Gábor M., Kiss, Brigitta, Cseklye, Judit, Drula, Elodie, Henrissat, Bernard, Nagy, István, Chovatia, Mansi, Adam, Catherine, LaButti, Kurt, Lipzen, Anna, Riley, Robert, Grigoriev, Igor V., and Nagy, László G. Mon . "Comparative genomics reveals unique wood-decay strategies and fruiting body development in the Schizophyllaceae". United States. https://doi.org/10.1111/nph.16032. https://www.osti.gov/servlets/purl/1619130.
@article{osti_1619130,
title = {Comparative genomics reveals unique wood-decay strategies and fruiting body development in the Schizophyllaceae},
author = {Almási, Éva and Sahu, Neha and Krizsán, Krisztina and Bálint, Balázs and Kovács, Gábor M. and Kiss, Brigitta and Cseklye, Judit and Drula, Elodie and Henrissat, Bernard and Nagy, István and Chovatia, Mansi and Adam, Catherine and LaButti, Kurt and Lipzen, Anna and Riley, Robert and Grigoriev, Igor V. and Nagy, László G.},
abstractNote = {Agaricomycetes are fruiting body-forming fungi that produce some of the most efficient enzyme systems to degrade wood. Despite decades-long interest in their biology, the evolution and functional diversity of both wood-decay and fruiting body formation are incompletely known. We performed comparative genomic and transcriptomic analyses of wood-decay and fruiting body development in Auriculariopsis ampla and Schizophyllum commune (Schizophyllaceae), species with secondarily simplified morphologies, an enigmatic wood-decay strategy and weak pathogenicity to woody plants. The plant cell wall-degrading enzyme repertoires of Schizophyllaceae are transitional between those of white rot species and less efficient wood-degraders such as brown rot or mycorrhizal fungi. Rich repertoires of suberinase and tannase genes were found in both species, with tannases restricted to Agaricomycetes that preferentially colonize bark-covered wood, suggesting potential complementation of their weaker wood-decaying abilities and adaptations to wood colonization through the bark. Fruiting body transcriptomes revealed a high rate of divergence in developmental gene expression, but also several genes with conserved expression patterns, including novel transcription factors and small-secreted proteins, some of the latter which might represent fruiting body effectors. Finally, taken together, our analyses highlighted novel aspects of wood-decay and fruiting body development in an important family of mushroom-forming fungi.},
doi = {10.1111/nph.16032},
journal = {New Phytologist},
number = 2,
volume = 224,
place = {United States},
year = {Mon Jul 01 00:00:00 EDT 2019},
month = {Mon Jul 01 00:00:00 EDT 2019}
}

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Enzyme Activity Profiles Produced on Wood and Straw by Four Fungi of Different Decay Strategies
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Hallmarks of Basidiomycete Soft- and White-Rot in Wood-Decay -Omics Data of Two Armillaria Species
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